Specifying the neurobiological basis of human attachment: brain, hormones, and behavior in synchronous and intrusive mothers

Abstract

The mother-infant bond provides the foundation for the infant's future mental health and adaptation and depends on the provision of species-typical maternal behaviors that are supported by neuroendocrine and motivation-affective neural systems. Animal research has demonstrated that natural variations in patterns of maternal care chart discrete profiles of maternal brain-behavior relationships that uniquely shape the infant's lifetime capacities for stress regulation and social affiliation. Such patterns of maternal care are mediated by the neuropeptide Oxytocin and by stress- and reward-related neural systems. Human studies have similarly shown that maternal synchrony--the coordination of maternal behavior with infant signals--and intrusiveness--the excessive expression of maternal behavior--describe distinct and stable maternal styles that bear long-term consequences for infant well-being. To integrate brain, hormones, and behavior in the study of maternal-infant bonding, we examined the fMRI responses of synchronous vs intrusive mothers to dynamic, ecologically valid infant videos and their correlations with plasma Oxytocin. In all, 23 mothers were videotaped at home interacting with their infants and plasma OT assayed. Sessions were micro-coded for synchrony and intrusiveness. Mothers were scanned while observing several own and standard infant-related vignettes. Synchronous mothers showed greater activations in the left nucleus accumbens (NAcc) and intrusive mothers exhibited higher activations in the right amygdala. Functional connectivity analysis revealed that among synchronous mothers, left NAcc and right amygdala were functionally correlated with emotion modulation, theory-of-mind, and empathy networks. Among intrusive mothers, left NAcc and right amygdala were functionally correlated with pro-action areas. Sorting points into neighborhood (SPIN) analysis demonstrated that in the synchronous group, left NAcc and right amygdala activations showed clearer organization across time, whereas among intrusive mothers, activations of these nuclei exhibited greater cross-time disorganization. Correlations between Oxytocin with left NAcc and right amygdala activations were found only in the synchronous group. Well-adapted parenting appears to be underlay by reward-related motivational mechanisms, temporal organization, and affiliation hormones, whereas anxious parenting is likely mediated by stress-related mechanisms and greater neural disorganization. Assessing the integration of motivation and social networks into unified neural activity that reflects variations in patterns of parental care may prove useful for the study of optimal vs high-risk parenting.

Figure 1

Header: (a) Experimental procedure. Footer: Mothers and infants were recruited 4–6 months post-partum and videotaped during a home visit. Video vignettes of mother–infant interaction were micro-coded for maternal synchrony and intrusiveness. Vignettes of interaction and of infant solitary play were used as functional magnetic resonance imaging (fMRI) stimuli. Header: (b) Experimental paradigm. Footer: Mothers were presented with infant-related vignettes of individually tailored stimuli of own infant and own mother–infant interaction (shown in red). Control stimuli of unfamiliar infants and interactions were fixed for all subjects and included stranger infants, typical mother–infant interaction, and pathological mother–infant interactions (shown in green). Each vignette was presented once and lasted 2 min. Clips were previewed by rest with fixation period of 1 min. Rest with fixation periods of 15–18 s were presented in between the films.

Figure 2

Header: Mean behavioral scores of synchrony and intrusiveness in synchronous and intrusive mothers. Footer: Among the synchronous mothers, the degree of synchrony was significantly higher than among the intrusive mothers (F=4.89, p=0.038). Among the intrusive mothers, the degree of intrusiveness was significantly higher than that in the synchronous group (F=8.98, p=0.0069). ^*p<0.05.

Figure 3

Header: Brain response to own infant video. Footer: Blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) statistical maps for 23 mothers presented with the contrast own infant (shown in orange)>stranger infant (shown in blue), showing activation in limbic areas such as the right nucleus accumbens and amygdala, and cortical activations such as the frontal, parietal temporal, and occipital gyri and insula.

Figure 4

Header: Region-of-Interest (ROI) signal analysis from nucleus accumbens (NAcc) and amygdala in synchronous and intrusive mothers. Footer: (a) Signal change was calculated as % from baseline, and then subtractions of stranger baby from own baby was preformed. A repeated measure 2 × 4 general linear model (GLM) revealed significant interaction effect (F_{(3, 57)}=3.8048, p=0.01480). Post hoc least significant difference (LSD) test mark the signal of left NAcc in synchronous moms as significantly higher than intrusive moms (p=0.015275), and also higher than the right amygdala of the same group (p=0.004939). Right amygdala's signal of intrusive moms were significantly higher than right amygdala's signal of synchronous moms (p=0.008181), which are higher than the left NA in the same group (trend, p=0.078460). (b) Correlation between Oxytocin plasma levels and left NAcc β weights in the contrast own infant>stranger infant are evident only in synchronous moms (N=14, r=0.7673, p=0.0014) and intrusive moms (N=6, r=−0.3877, p=0.4475). (c) Correlation between Oxytocin plasma levels and right amygdala β weights in the contrast own infant>stranger infant are evident only in synchronous moms (r=0.6490, p=0.012) and intrusive moms (r=0.5863, p=0.2213), not shown. (d) Sorting points into neighborhood (SPIN) analysis. Synchrony clustering according to the activation time course of the left NAcc. (e) SPIN analysis. Synchrony clustering according to the activation time course of the right amygdala. Mothers were presented with infant-related vignettes of individually tailored stimuli of own infant and own mother–infant interaction (shown in red). Control stimuli of unfamiliar infants and interactions were fixed for all subjects and included stranger infants, typical mother–infant interaction, and pathological mother–infant interactions (shown in green). An intrusive mother in the intrusive cluster is marked with red ‘I'. A synchronous mother in the synchrony cluster is marked with orange ‘S'. Mothers who appear outside of their cluster are marked with a black initial. ^*p<0.05.

Figure 5

Header: Inter-regional functional connectivity analysis from left nucleus accumbens (NAcc) and right amygdala in synchronous (N=13) and intrusive mothers (N=10), random effect. Footer: (a) A whole brain t-test between groups with left NAcc as seed region show significantly higher functional correlation with paracingulate medial prefrontal cortex (PFC) among synchronous moms than among intrusive moms. (b) A whole brain t-test between groups with right amygdala as seed region showing significantly higher functional correlation in orbito-frontal cortex (OFC) and pre-supplementary motor area (pre-SMA) among intrusive moms than synchronous moms. Synchronous moms display amygdala correlation to inferior frontal gyrus (IFG), superior temporal gyrus (STG), and insula.